Evidence for lower plasticity in CTMAX at warmer developmental temperatures

Understanding the capacity for different species to reduce their susceptibility to climate change via phenotypic plasticity is essential for accurately predicting species extinction risk. The climatic variability hypothesis suggests that spatial and temporal variation in climatic variables should select for more plastic phenotypes. However, empirical support for this hypothesis is limited. Here, we examine the capacity for ten Drosophila species to increase their critical thermal maxima (CT_MAX) through developmental acclimation and/or adult heat hardening. Using four fluctuating developmental temperature regimes, ranging from 13 to 33 °C, we find that most species can increase their CT_MAX via developmental acclimation and adult hardening, but found no relationship between climatic variables and absolute measures of plasticity. However, when plasticity was dissected across developmental temperatures, a positive association between plasticity and one measure of climatic variability (temperature seasonality) was found when development took place between 26 and 28 °C, whereas a negative relationship was found when development took place between 20 and 23 °C. In addition, a decline in CT_MAX and egg‐to‐adult viability, a proxy for fitness, was observed in tropical species at the warmer developmental temperatures (26–28 °C); this suggests that tropical species may be at even greater risk from climate change than currently predicted. The combined effects of developmental acclimation and adult hardening on CT_MAX were small, contributing to a <0.60 °C shift in CT_MAX. Although small shifts in CT_MAX may increase population persistence in the shorter term, the degree to which they can contribute to meaningful responses in the long term is unclear.     

Local genetic adaptation generates latitude‐specific effects of warming on predator–prey interactions

Temperature effects on predator–prey interactions are fundamental to better understand the effects of global warming. Previous studies never considered local adaptation of both predators and prey at different latitudes, and ignored the novel population combinations of the same predator–prey species system that may arise because of northward dispersal. We set up a common garden warming experiment to study predator–prey interactions between Ischnura elegans damselfly predators and Daphnia magna zooplankton prey from three source latitudes spanning >1500 km. Damselfly foraging rates showed thermal plasticity and strong latitudinal differences consistent with adaptation to local time constraints. Relative survival was higher at 24 °C than at 20 °C in southern Daphnia and higher at 20 °C than at 24 °C, in northern Daphnia indicating local thermal adaptation of the Daphnia prey. Yet, this thermal advantage disappeared when they were confronted with the damselfly predators of the same latitude, reflecting also a signal of local thermal adaptation in the damselfly predators. Our results further suggest the invasion success of northward moving predators as well as prey to be latitude‐specific. We advocate the novel common garden experimental approach using predators and prey obtained from natural temperature gradients spanning the predicted temperature increase in the northern populations as a powerful approach to gain mechanistic insights into how community modules will be affected by global warming. It can be used as a space‐for‐time substitution to inform how predator–prey interaction may gradually evolve to long‐term warming.     

Whole‐genome resequencing reveals the pleistocene temporal dynamics of Branchiostoma belcheri and Branchiostoma floridae populations

Global climatic fluctuations governed the ancestral demographic histories of species and contributed to place the current population status into a more extensive ecological and evolutionary context. Genetic variations will leave unambiguous signatures in the patterns of intraspecific genetic variation in extant species since the genome of each individual is an imperfect mosaic of the ancestral genomes. Here, we report the genome sequences of 20 Branchiostoma individuals by whole‐genome resequencing strategy. We detected over 140 million genomic variations for each Branchiostoma individual. In particular, we applied the pairwise sequentially Markovian coalescent (PSMC) method to estimate the trajectories of changes in the effective population size (N_e) of Branchiostoma population during the Pleistocene. We evaluated the threshold of sequencing depth for proper inference of demographic histories using PSMC was ≥25×. The PSMC results highlight the role of historical global climatic fluctuations in the long‐term population dynamics of Branchiostoma. The inferred ancestral N_e of the Branchiostoma belcheri populations from Zhanjiang and Xiamen (China) seawaters was different in amplitude before the first (mutation rate = 3 × 10^?9) or third glaciation (mutation rate = 9 × 10^?9) of the Pleistocene, indicating that the two populations most probably started to evolve in isolation in their respective seas after the first or third glaciation of the Pleistocene. A pronounced population bottleneck coinciding with the last glacial maximum was observed in all Branchiostoma individuals, followed by a population expansion occurred during the late Pleistocene. Species that have experienced long‐term declines may be especially vulnerable to recent anthropogenic activities. Recently, the industrial pollution and the exploitation of sea sand have destroyed the harmonious living environment of amphioxus species. In the future, we need to protect the habitat of Branchiostoma and make full use of these detected genetic variations to facilitate the functional study of Branchiostoma for adaptation to local environments.     

Host‐specific thermal profiles affect fitness of a widespread pathogen

Host behavior can interact with environmental context to influence outcomes of pathogen exposure and the impact of disease on species and populations. Determining whether the thermal behaviors of individual species influence susceptibility to disease can help enhance our ability to explain and predict how and when disease outbreaks are likely to occur. The widespread disease chytridiomycosis (caused by the fungal pathogen Batrachochytrium dendrobatidis, Bd) often has species‐specific impacts on amphibian communities; some host species are asymptomatic, whereas others experience mass mortalities and population extirpation. We determined whether the average natural thermal regimes experienced by sympatric frog species in nature, in and of themselves, can account for differences in vulnerability to disease. We did this by growing Bd under temperatures mimicking those experienced by frogs in the wild. At low and high elevations, the rainforest frogs Litoria nannotis, L. rheocola, and L. serrata maintained mean thermal regimes within the optimal range for pathogen growth (15–25°C). Thermal regimes for L. serrata, which has recovered from Bd‐related declines, resulted in slower pathogen growth than the cooler and less variable thermal regimes for the other two species, which have experienced more long‐lasting declines. For L. rheocola and L. serrata, pathogen growth was faster in thermal regimes corresponding to high elevations than in those corresponding to low elevations, where temperatures were warmer. For L. nannotis, which prefers moist and thermally stable microenvironments, pathogen growth was fastest for low‐elevation thermal regimes. All of the thermal regimes we tested resulted in pathogen growth rates equivalent to, or significantly faster than, rates expected from constant‐temperature experiments. The effects of host body temperature on Bd can explain many of the broad ecological patterns of population declines in our focal species, via direct effects on pathogen fitness. Understanding the functional response of pathogens to conditions experienced by the host is important for determining the ecological drivers of disease outbreaks.     

Ecological change predicts population dynamics and genetic diversity over 120 000 years

While ecological effects on short‐term population dynamics are well understood, their effects over millennia are difficult to demonstrate and convincing evidence is scant. Using coalescent methods, we analysed past population dynamics of three lizard species (Psammodromus hispanicus, P. edwardsianus, P. occidentalis) and linked the results with climate change data covering the same temporal horizon (120 000 years). An increase in population size over time was observed in two species, and in P. occidentalis, no change was observed. Temporal changes in temperature seasonality and the maximum temperature of the warmest month were congruent with changes in population dynamics observed for the three species and both variables affected population density, either directly or indirectly (via a life‐history trait). These results constitute the first solid link between ecological change and long‐term population dynamics. The results moreover suggest that ecological change leaves genetic signatures that can be retrospectively traced, providing evidence that ecological change is a crucial driver of genetic diversity and speciation.     

Use of field‐portable ultrasonography reveals differences in developmental phenology and maternal egg provisioning in two sympatric viviparous snakes

A thorough understanding of the life cycles underlying the demography of wild species is limited by the difficulty of observing hidden life‐history traits, such as embryonic development. Major aspects of embryonic development, such as the rate and timing of development, and maternal–fetal interactions can be critical features of early‐life fitness and may impact population trends via effects on individual survival. While information on development in wild snakes and lizards is particularly limited, the repeated evolution of viviparity and diversity of reproductive mode in this clade make it a valuable subject of study. We used field‐portable ultrasonography to investigate embryonic development in two sympatric garter snake species, Thamnophis sirtalis and Thamnophis elegans in the Sierra Nevada mountains of California. This approach allowed us to examine previously hidden reproductive traits including the timing and annual variation in development and differences in parental investment in young. Both species are viviparous, occupy similar ecological niches, and experience the same annual environmental conditions. We found that T. sirtalis embryos were more developmentally advanced than T. elegans embryos during June of three consecutive years. We also found that eggs increased in volume more substantially across developmental stages in T. elegans than in T. sirtalis, indicating differences in maternal provisioning of embryos via placental transfer of water. These findings shed light on interspecific differences in parental investment and timing of development within the same environmental context and demonstrate the value of field ultrasonography for pursuing questions relating to the evolution of reproductive modes, and the ecology of development.     

Long‐term panmixia in a cosmopolitan Indo‐Pacific coral reef fish and a nebulous genetic boundary with its broadly sympatric sister species

Phylogeographical studies have shown that some shallow‐water marine organisms, such as certain coral reef fishes, lack spatial population structure at oceanic scales, despite vast distances of pelagic habitat between reefs and other dispersal barriers. However, whether these dispersive widespread taxa constitute long‐term panmictic populations across their species ranges remains unknown. Conventional phylogeographical inferences frequently fail to distinguish between long‐term panmixia and metapopulations connected by gene flow. Moreover, marine organisms have notoriously large effective population sizes that confound population structure detection. Therefore, at what spatial scale marine populations experience independent evolutionary trajectories and ultimately species divergence is still unclear. Here, we present a phylogeographical study of a cosmopolitan Indo‐Pacific coral reef fish Naso hexacanthus and its sister species Naso caesius, using two mtDNA and two nDNA markers. The purpose of this study was two‐fold: first, to test for broad‐scale panmixia in N. hexacanthus by fitting the data to various phylogeographical models within a Bayesian statistical framework, and second, to explore patterns of genetic divergence between the two broadly sympatric species. We report that N. hexacanthus shows little population structure across the Indo‐Pacific and a range‐wide, long‐term panmictic population model best fit the data. Hence, this species presently comprises a single evolutionary unit across much of the tropical Indian and Pacific Oceans. Naso hexacanthus and N. caesius were not reciprocally monophyletic in the mtDNA markers but showed varying degrees of population level divergence in the two nuclear introns. Overall, patterns are consistent with secondary introgression following a period of isolation, which may be attributed to oceanographic conditions of the mid to late Pleistocene, when these two species appear to have diverged.     

Decadal losses of canopy‐forming algae along the warm temperate coastline of Brazil

The loss of canopy‐forming seaweeds from urbanized coasts has intensified in response to warming seas and non‐climatic pressures such as population growth and declining water quality. Surprisingly, there has been little information on the extent of historical losses in the South‐western Atlantic, which limits our ability to place this large marine ecosystem in a global context. Here, we use meta‐analysis to examine long‐term (1969–2017) changes to the cover and biomass of Sargassum spp. and structurally simple algal turfs along more than 1,000 kilometres of Brazil's warm temperate coastline. Analysis revealed major declines in canopy cover that were independent of season (i.e., displaying similar trends for both summer and winter) but varied with coastal environmental setting, whereby sheltered bays experienced greater losses than coastal locations. On average, covers of Sargassum spp. declined by 2.6% per year, to show overall losses of 52% since records began (ranging from 20% to 89%). This contrasted with increases in the cover of filamentous turfs (24% over the last 27 years) which are known to proliferate along human‐impacted coasts. To test the relative influence of climatic versus non‐climatic factors as drivers of this apparent canopy‐to‐turf shift, we examined how well regional warming trends (decadal changes to sea surface temperature) and local proxies of coastal urbanization (population density, thermal pollution, turbidity and nutrient inputs) were able to predict the changes in seaweed communities. Our results revealed that the most pronounced canopy losses over the past 50 years were at sites exhibiting the greatest degree of coastal warming, the highest population growth and those located in semi‐enclosed sheltered bays. These findings contribute knowledge on the drivers of canopy loss in the South‐western Atlantic and join with global efforts to understand and mitigate declines of marine keystone species.     

Experimental evidence of genome‐wide impact of ecological selection during early stages of speciation‐with‐gene‐flow

Theory predicts that speciation‐with‐gene‐flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome‐wide impacts of host‐associated selection between hawthorn and apple host races of Rhagoletis pomonella (Diptera: Tephritidae), a model for contemporary speciation‐with‐gene‐flow. Allele frequency shifts of 32 455 SNPs induced in a selection experiment based on host phenology were genome wide and highly concordant with genetic divergence between co‐occurring apple and hawthorn flies in nature. This striking genome‐wide similarity between experimental and natural populations of R. pomonella underscores the importance of ecological selection at early stages of divergence and calls for further integration of studies of eco‐evolutionary dynamics and genome divergence.     

Long‐term ecological data for conservation: Range change in the black‐billed capercaillie (Tetrao urogalloides) in northeast China (1970s–2070s)

Long‐term ecological data can be an effective tool to help ecologists integrate future projections with historical contexts and provide unique insights into the long‐term dynamics of endangered species. However, hampered by data limitations, including incomplete and spatially biased data, relatively few studies have used multidecadal datasets or have examined changes in biogeography from a historical perspective. The black‐billed capercaillie (Tetrao urogalloides) is a large capercaillie (classified as Least Concern [LC] on the IUCN red list) that has undergone a dramatic decline in population during the late 20th century and is considered endangered. Its conservation status is pessimistic, and the species requires immediate protection. Therefore, we supplemented a historical dataset to identify changes in this bird's range and population in northeast China over the long term. The study area spanned Heilongjiang Province, Jilin Province, and the northeast corner of Inner Mongolia in northeast China. We integrated an ecological niche model (BIOMOD2) with long‐term ecological data on this species to estimate the magnitude of change in distribution over time. Our results revealed a 35.25% reduction in the current distribution of this species compared to their potential distribution in the 1970s. This decline is expected to continue under climate change. For example, the future range loss was estimated to be 38.79 ± 0.22% (8.64–90.19%), and the actual state could be worse, because the baseline range of the model was greater than the real range in the 2000s, showing a 12.39% overestimation. To overcome this poor outlook, a conservation strategy should be established in sensitive areas, including the southwestern Greater Khingan Mountains and northern Lesser Khingan Mountains. Actions that should be considered include field investigations, establishing a monitor network, designing ecological corridors, and cooperating with local inhabitants, governments, and conservation biologists to improve the conservation of the black‐billed capercaillie.     

The crayfish plague pathogen can infect freshwater‐inhabiting crabs

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Density‐dependent and density‐independent drivers of population change in Barton Springs salamanders

Understanding population change is essential for conservation of imperiled species, such as amphibians. Worldwide amphibian declines have provided an impetus for investigating their population dynamics, which can involve both extrinsic (density‐independent) and intrinsic (density‐dependent) drivers acting differentially across multiple life stages or age classes. In this study, we examined the population dynamics of the endangered Barton Springs Salamander (Eurycea sosorum) using data from a long‐term monitoring program. We were interested in understanding both the potential environmental drivers (density‐independent factors) and demographic factors (interactions among size classes, negative density dependence) to better inform conservation and management activities. We used data from three different monitoring regimes and multivariate autoregressive state‐space models to quantify environmental effects (seasonality, discharge, algae, and sediment cover), intraspecific interactions among three size classes, and intra‐class density dependence. Results from our primary data set revealed similar patterns among sites and size classes and were corroborated by our out‐of‐sample data. Cross‐correlation analysis showed juvenile abundance was most strongly correlated with a 9‐month lag in aquifer discharge, which we suspect is related to inputs of organic carbon into the aquifer. However, sedimentation limited juvenile abundance at the surface, emphasizing the importance of continued sediment management. Recruitment from juveniles to the sub‐adult size class was evident, but negative density‐dependent feedback ultimately regulated each size class. Negative density dependence may be an encouraging sign for the conservation of E. sosorum because populations that can reach carrying capacity are less likely to go extinct compared to unregulated populations far below their carrying capacity. However, periodic population declines coupled with apparent migration into the aquifer complicate assessments of species status. Although both density‐dependent and density‐independent drivers of population change are not always apparent in time series of animal populations, both have important implications for conservation and management of E. sosorum.     

Time‐specific and pleiotropic quantitative trait loci coordinately modulate stem growth in Populus

In perennial woody plants, the coordinated increase of stem height and diameter during juvenile growth improves competitiveness (i.e. access to light); however, the factors underlying variation in stem growth remain unknown in trees. Here, we used linkage‐linkage disequilibrium (linkage‐LD) mapping to decipher the genetic architecture underlying three growth traits during juvenile stem growth. We used two Populus populations: a linkage mapping population comprising a full‐sib family of 1,200 progeny and an association mapping panel comprising 435 unrelated individuals from nearly the entire natural range of Populus tomentosa. We mapped 311 quantitative trait loci (QTL) for three growth traits at 12 timepoints to 42 regions in 17 linkage groups. Of these, 28 regions encompassing 233 QTL were annotated as 27 segmental homology regions (SHRs). Using SNPs identified by whole‐genome re‐sequencing of the 435‐member association mapping panel, we identified significant SNPs (P ≤ 9.4 × 10^?7) within 27 SHRs that affect stem growth at nine timepoints with diverse additive and dominance patterns, and these SNPs exhibited complex allelic epistasis over the juvenile growth period. Nineteen genes linked to potential causative alleles that have time‐specific or pleiotropic effects, and mostly overlapped with significant signatures of selection within SHRs between climatic regions represented by the association mapping panel. Five genes with potential time‐specific effects showed species‐specific temporal expression profiles during the juvenile stages of stem growth in five representative Populus species. Our observations revealed the importance of considering temporal genetic basis of complex traits, which will facilitate the molecular design of tree ideotypes.     

Fluctuating thermal environments and time‐dependent effects on fruit fly egg‐hatching performance

Organismal performance in a changing environment is dependent on temporal patterns and duration of exposure to thermal variability. We experimentally assessed the time‐dependent effects of thermal variability (i.e., patterns of thermal exposure) on the hatching performance of Drosophila melanogaster. Flies were collected in central Chile and maintained for four generations in laboratory conditions. Fourth generation eggs were acclimated to different thermal fluctuation cycles until hatching occurred. Our results show that the frequency of extreme thermal events has a significant effect on hatching success. Eggs exposed to 24 hr cycles of thermal fluctuation had a higher proportion of eggs that hatched than those acclimated to shorter (6 and 12 hr) and longer cycles (48 hr). Furthermore, eggs subjected to frequent thermal fluctuations hatched earlier than those acclimated to less frequent thermal fluctuations. Overall, we show that, egg‐to‐adult viability is dependent on the pattern of thermal fluctuations experienced during ontogeny; thus, the pattern of thermal fluctuation experienced by flies has a significant and until now unappreciated impact on fitness.     

Differential expression patterns of two delta‐9‐acyl‐CoA desaturases in Thitarodes pui (Lepidoptera: Hepialidae) during different seasons and cold exposure

Thitarodes pui larvae have a limited distribution in the Tibetan Plateau and are the host of a parasitic fungus, Ophiocordyceps sinensis. Low temperature is a main environmental stress. However, understanding of T. pui cold adaptation mechanisms is insufficient. Delta‐9‐acyl‐CoA desaturase (D9D) is closely correlated with cold adaptation for many organisms. To further understand the cold adaptation processes in T. pui larvae, two D9Ds, TpdesatA and TpdesatB were sequenced, and expression patterns were investigated during different seasons and cold exposure (under 0°C) in the laboratory. The full lengths of two cDNAs are 1,290 bp and 1,603 bp, and the ORFs encode a polypeptide of 348 and 359 amino acids, respectively. Four transmembrane domains, three conserved histidine residues and five hydrophobic regions exist in these two sequences. The expression level of TpdesatA is up‐regulated in the long‐term cold exposure and negatively correlated with temperature in seasonal patterns. TpdesatB responds to cold temperature in short‐term cold exposure and positively corresponds temporarily in seasonal expression. Two D9Ds may have different substrate specificities, TpdesatA tends to use C16:0 and C18:0 as substrate while TpdesatB prefers C18:0. In conclusion, TpdesatA may play a very important role in T. pui cold tolerance and TpdesatB regulates function in short‐term cold exposure and content change of fatty acids in the body.     

Carry‐over effects of multiple stressors on benthic embryos are mediated by larval exposure to elevated UVB and temperature

Damaging effects of UVB in conjunction with other stressors associated with global change are well‐established, with many studies focused on vulnerable early life stages and immediate effects (e.g., mortality, developmental abnormalities). However, for organisms with complex life cycles, experiences at one life stage can have carry‐over effects on later life stages, such that sublethal effects may mediate later vulnerability to further stress. Here, we exposed embryos in benthic egg masses of the New Zealand intertidal gastropod Siphonaria australis to treatments of either periodic stress (e.g., elevated UVB, salinity, and water temperature mimicking tidepool conditions in which egg masses are commonly found during summer) or control conditions (low UVB, ambient salinity, and water temperatures). Although there was high mortality from stressed egg masses, 24% of larvae hatched successfully. We then exposed the hatching larvae from both egg mass treatments to different combinations of water temperature (15 or 20 °C) and light (high UVB or shade) 12 h per day for 10 days. The most stressful larval conditions of 20 °C/high UVB resulted in low survival and stunted growth. Carry‐over effects on survival were apparent for shaded larvae exposed to elevated temperature, where those from stressed egg masses had 1.8× higher mortality than those from control egg masses. Shaded larvae were also larger and had longer velar cilia if they were from control egg masses, independent of larval temperature. These results demonstrate that previous experience of environmental stress can influence vulnerability of later life stages to further stress, and that focus on a single life stage will underestimate cumulative effects of agents of global change.     

An anthropogenic habitat within a suboptimal colonized ecosystem provides improved conditions for a range‐shifting species

Many species are shifting their ranges in response to the changing climate. In cases where such shifts lead to the colonization of a new ecosystem, it is critical to establish how the shifting species itself is impacted by novel environmental and biological interactions. Anthropogenic habitats that are analogous to the historic habitat of a shifting species may play a crucial role in the ability of that species to expand or persist in suboptimal colonized ecosystems. We tested if the anthropogenic habitat of docks, a likely mangrove analog, provides improved conditions for the range‐shifting mangrove tree crab Aratus pisonii within the colonized suboptimal salt marsh ecosystem. To test if docks provided an improved habitat, we compared the impact of the salt marsh and dock habitats on ecological and life history traits that influence the ability of this species to persist and expand into the salt marsh and compared these back to baselines in the historic mangrove ecosystem. Specifically, we examined behavior, physiology, foraging, and the thermal conditions of A. pisonii in each habitat. We found that docks provide a more favorable thermal and foraging habitat than the surrounding salt marsh, while their ability to provide conditions which improved behavior and physiology was mixed. Our study shows that anthropogenic habitats can act as analogs to historic ecosystems and enhance the habitat quality for range‐shifting species in colonized suboptimal ecosystems. If the patterns that we document are general across systems, then anthropogenic habitats may play an important facilitative role in the range shifts of species with continued climate change.